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Direct nitrous oxide emissions in Mediterranean climatecropping systems: Emission factors based on ameta-analysis of available measurement data

Maria L Cayuela, Eduardo Aguilera, Alberto Sanz-Cobena, Dean C Adams,Diego Abalos, Louise Barton, Rebecca Ryals, Whendee L Silver, Marta A

Alfaro, Valentini A Pappa, et al.

To cite this version:Maria L Cayuela, Eduardo Aguilera, Alberto Sanz-Cobena, Dean C Adams, Diego Abalos, et al..Direct nitrous oxide emissions in Mediterranean climate cropping systems: Emission factors based ona meta-analysis of available measurement data. Agriculture, Ecosystems and Environment, ElsevierMasson, 2017, 238, pp.25 - 35. �10.1016/j.agee.2016.10.006�. �hal-01771776�

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Direct nitrous oxide emissions in Mediterranean climate cropping systems: Emission

factors based on a meta-analysis of available measurement data

Maria L. Cayuelaa,*, Eduardo Aguilerab, Alberto Sanz-Cobenac, Dean C. Adamsd,e, Diego Abalosf, Louise Bartong,

Rebecca Ryalsh, Whendee L. Silveri, Marta A. Alfaroj, Valentini A. Pappak,l, Pete Smithm, Josette Garniern, Gilles

Billenn, Lex Bouwmano,p, Alberte Bondeauq, Luis Lassalettao

a Departamento de Conservación de Suelos y Aguas y Manejo de Residuos Orgánicos, CEBAS-CSIC, Campus

Universitario de Espinardo, 30100 Murcia, Spain

b Universidad Pablo de Olavide, Ctra. de Utrera, km. 1, 41013, Sevilla, Spain

c ETSI Agronomos, Technical University of Madrid, Ciudad Universitaria, 28040 Madrid, Spain

d Department of Ecology, Evolution, and Organismal Biology, Iowa State University, Ames, IA 50010, USA

e Department of Statistics, Iowa State University, Ames, IA 50010, USA

f Department of Soil Quality, Wageningen University, PO Box 47, Droevendaalsesteeg 4, Wageningen 6700AA,

The Netherlands

g Soil Biology and Molecular Ecology Group, School of Earth and Environment, UWA Institute of Agriculture,

Faculty of Science, The University of Western Australia, 35 Stirling Highway, Crawley WA 6009, Australia

h Department of Natural Resources and Environmental Management, University of Hawaii, Manoa, Honolulu

HI, 96822, USA

i Department of Environmental Science, Policy, and Management, University of California, Berkeley, CA 94707,

USA

j Instituto de Investigaciones Agropecuarias, Centro Regional de Investigación Remehue, Casilla 24-O, Osorno,

Chile

k Agricultural University of Athens, Department of Crop Science, Iera Odos 75, 11855 Athens, Greece

l Texas A&M University, 302H Williams Administration Bldg, College Station, TX 77843-3372, USA

m Institute of Biological and Environmental Sciences, University of Aberdeen, 23 St Machar Drive, Aberdeen,

AB24 3UU, UK

n Sorbonne Universités, Univ Paris 06, CNRS, EPHE, UMR 7619 METIS, 4 place Jussieu, 75005 PARIS, France

o PBL Netherlands Environmental Assessment Agency, PO Box 303314, 2500 GH The Hague, The Netherlands

p Department of Earth Sciences – Faculty of Geosciences, Utrecht University, PO Box 80021, 3508 TA Utrecht,

The Netherlands

q Institut Méditerranéen de Biodiversité et d’Ecologie marine et continentale (IMBE) Aix Marseille Université,

CNRS, IRD, Avignon Université, Aix-en-Provence, France

Corresponding author. E-mail addresses: mlcayuela@cebas.csic.es, marialuz.cayuela@gmail.com,

marialuz.cayuela@yahoo.es (M.L. Cayuela).

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Abstract

Many recent reviews and meta-analyses of N2O emissions do not include data from Mediterranean studies. In

this paper we present a meta-analysis of the N2O emissions from Mediterranean cropping systems, and

propose a more robust and reliable regional emission factor (EF) for N2O, distinguishing the effects of water

management, crop type, and fertilizer management. The average overall EF for Mediterranean agriculture

(EFMed) was 0.5%, which is substantially lower than the IPCC default value of 1%. Soil properties had no

significant effect on EFs for N2O. Increasing the N fertilizer rate led to higher EFs; when N was applied at rates

greater than 400 kg N ha-1, the EF did not significantly differ from the 1% default value (EF: 0.82%). Liquid

slurries led to emissions that did not significantly differ from 1%; the other fertilizer types were lower but did

not significantly differ from each other. Rain-fed crops in Mediterranean regions have lower EFs (EF: 0.27%)

than irrigated crops (EF: 0.63%). Drip irrigation systems (EF: 0.51%) had 44% lower EF than sprinkler irrigation

methods (EF: 0.91%). Extensive crops, such as winter cereals (wheat, oat and barley), had lower EFs (EF: 0.26%)

than intensive crops such as maize (EF: 0.83%). For flooded rice, anaerobic conditions likely led to complete

denitrification and low EFs (EF: 0.19%). Our results indicate that N2O emissions from Mediterranean agriculture

are overestimated in current national greenhouse gas inventories and that, with the new EF determined from

this study, the effect of mitigation strategies such as drip irrigation or the use of nitrification inhibitors, even if

highly significant, may be smaller in absolute terms.

Keywords: N2O, Greenhouse gases, Field studies, Mitigation, Systematic review

1. Introduction

More than half of the global Mediterranean climate zone is located on the Mediterranean Sea Basin

(Aschmann, 1973); the remainder is on the Pacific coast of North America, south-western Australia, the Cape

region of South Africa and the central coast of Chile (Olson et al., 2001). One of the most distinctive features of

Mediterranean climates is the summer drought and relatively mild temperatures in winter. However, annual

precipitation is variable, between 275 and 1000 mm, such that Mediterranean climate regions range from

semi-arid to humid.

In Mediterranean climates, precipitation and temperatures are suitable in winter for cultivating a variety of

rain-fed crops including cereals, grain legumes, oilseeds and horticulture (Andrews et al., 2002). Cultivation of

perennial crops is common in Mediterranean climate areas. Some of these crops are resistant to summer

droughts, including olives, almonds, and grapes, while others are cultivated under irrigation, such as citrus and

other fruit trees. Agriculture in Mediterranean climates regions, therefore, provides a high diversity of crops.

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Agricultural soils are regarded as the primary source of anthropogenic N2O emissions (Smith et al., 2008).

Despite the cultural and economic importance of Mediterranean agriculture (Grigg, 1974), the number of field

studies analyzing N2O emissions from Mediterranean agricultural lands is much smaller than from other

temperate areas (Stehfest and Bouwman, 2006). Recent reviews and meta-analyses of N2O emissions do not

include data from Mediterranean studies (e.g. Kim et al., 2013; Lesschen et al., 2011; Shcherbak et al., 2014).

Estimating N2O emissions and N2O emission factors (EF, the percentage of fertilizer N applied that is

transformed and emitted on site as N2O) is essential for assessing the impact of agriculture on greenhouse gas

(GHG) emissions for a particular area. Current national emission inventory methods use a direct EF for N2O,

with a default value of 1% or 1.25% (depending on the country) of the N input from manure and mineral

fertilizer (IPCC, 2006). However, many studies have concluded that the response of direct N2O emissions to N

input is non-linear (Kim et al., 2013; Philibert et al., 2012; Shcherbak et al., 2014), and other recent studies

highlighted the important role of environmental and management factors in determining N2O emissions and

EFs, such as climate, soil characteristics, type of fertilizer and time of application, crop type, and irrigation

system (Aguilera et al., 2013a; Bouwman et al., 2002; Gerber et al., 2016; Leip et al., 2011; Lesschen et al.,

2011). For example, Aguilera et al. (2013a) suggested using a lower EF for Mediterranean areas than for other

temperate regions, especially in rain-fed systems.

There are three characteristics of Mediterranean regions that are fundamental to understanding why soil N2O

emissions from these regions are idiosyncratic and in-turn why the adoption of EFs which differ from other

climate regions should be considered. Firstly, due to limited availability of water, irrigation is a prerequisite for

the cultivation of many annual crops during summer, whereas mild, humid winters enable annual crops to be

rain-fed. Different EFs are therefore needed for irrigated and rain-fed crops. Secondly, soils in the

Mediterranean zone generally have a neutral to alkaline soil pH and very low concentrations of organic C

(Aguilera et al., 2013b; Verheye and de la Rosa, 2005). These conditions influence denitrification rates and

N2O/N2 ratios (Li et al., 2005; Šimek and Cooper, 2002). Thirdly, soils in Mediterranean regions are rarely

exposed to freeze–thaw cycles, which cause high N2O emissions, especially in fertilized soils (Schouten et al.,

2012; Tenuta and Sparling, 2011), which lead to high EFs.

The aim of this study was to improve our understanding of soil N2O emissions from Mediterranean cropping

systems by (i) summarizing available field data of soil N2O emissions; (ii) proposing a more robust and reliable

regional EF; and (iii) identifying controlling factors of N2O EFs (soil type, climate variability, irrigation and N

fertilizer management) as a basis for developing soil N2O mitigation strategies for regions with Mediterranean

climates.

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Fig. 1. Location of the study sites included in the dataset. The dark gray area delimits the Mediterranean biome from the collection of ecoregions mapped by the World Wildlife Fund (Olson et al., 2001).

2. Methods

2.1. Selection of studies and data extraction

There are varying definitions to demarcate Mediterranean climate regions worldwide, which are typically

based on climate and plant associations. We chose the widely used delineation of the Mediterranean biome

from the collection of ecoregions mapped by the World Wildlife Fund (Fig. 1). We selected studies in this area

and in marginal areas defined as ‘Mediterranean’ by the authors of the original papers. Soil N2O emission data

from field-based studies investigating fertilizer-induced soil N2O emissions were collected from these

Mediterranean regions, including the Mediterranean Sea Basin, California, Australia and Chile (Fig. 1). We are

not aware of any field study reporting N2O emissions in the Mediterranean region of South Africa (Mary

Scholes, Wits University, personal communication).

The criteria for inclusion of a study in the dataset were: (i) area-scaled N2O emissions were reported for N

fertilizer treatments, (ii) the number of replicates was reported unambiguously with a minimum of three

replicates per treatment, (iii) only field studies were considered and (iv) only when N2O emissions were

reported for at least an entire growing season.

The cumulative N2O emissions for each N fertilizer treatment were extracted from published papers and

reports, together with a measure of variance, the number of replicates and the N application rate (kg N ha-1)

during the observational period. Key characteristics (location, climate data, soil type, soil management,

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irrigation, type of fertilizers, etc.) were collected when available (Supplementary material 1). When data were

presented graphically, WebPlot Digitizer was used to extract data points (http://

arohatgi.info/WebPlotDigitizer/). If cumulative N2O emissions or other information were not reported, the

authors of the field study were contacted to supply missing information. In some cases, cumulative emissions

were estimated by integrating the average daily fluxes over the measurement period (Alluvione et al., 2010;

Castaldi et al., 2011; Kong et al., 2009; Ranucci et al., 2011; Vitale et al., 2013). Experiments assessing the

effect of nitrification/ urease inhibitors were studied as a separate group (when evaluating the influence of the

type of fertilization), but were not included to obtain the mean EF for Mediterranean crops(EFMed) because

they were not considered representative of current management practices. Fifty-three studies and 223 data-

sets were included in the meta-analyses (Table 1, Supplementary material 1).

Since most of the field studies in our database focus on assessing the performance of specific crop

management practices over both emissions and crop yields, they often do not include post-harvest season

emissions. While full year emissions are desirable for determining EFs (IPCC, 2016), in the systems we are

studying, we assume that the inclusion of growing season only emissions will have minimal influence on our

calculated EFs, since emissions in the intercrop period will be a) low in summer (fallow of winter crops), when

the soil is dry, due to decreased microbiological activity, and b) very low in winter (fallow of summer crops)

under cold conditions without freeze–thaw cycles (Aguilera et al., 2013a). In the few studies where emissions

were measured over an entire year, those during the fallow period were 10% or less of the total (e.g. Sanz-

Cobena et al., 2012).

Table 1 Studies included in the meta-analyses.

Mediterranean-type climate area

Country Studies

Mediterranean Basin

Spain Abalos et al. (2012, 2013, 2014); Huérfano et al. (2015); López-Fernández et al. (2007); Maris et al. (2015a, 2015b); Meijide et al. (2007, 2009); Plaza-Bonilla et al. (2014); Sánchez-García et al. (2016); Sánchez-Martín et al. (2008, 2010a, 2010b); Sanz-Cobena et al. (2012, 2014a); Tellez-Rio et al. (2015); Vallejo et al. (2005, 2006, 2014)

Italy Alluvione et al. (2010); Bosco et al. (2015); Castaldi et al. (2011); Ranucci et al. (2011); Rees et al. (2013); Vitale et al. (2013)

Israel/Portugal/Greece

Heller et al. (2010); Kontopoulou et al. (2015); Pereira et al. (2013)

Australia Australia Barton et al. (2008, 2010, 2013); Li et al. (2011)

California USA Alsina et al. (2013); Angst et al. (2014); Garland et al. (2011, 2014); Kallenbach et al. (2010); Kennedy et al. (2013); Kong et al. (2009); Lee et al. (2009); Pittelkow et al. (2013); Schellenberg et al. (2012); Simmonds et al. (2015); Suddick and Six (2013); Townsend-Small et al. (2011); Verhoeven and Six (2014); Zhu-Barker et al. (2015)

Chile Chile Hube et al. (2017); Vistoso et al. (2012)

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2.2. Soil and land management data compilation

Soil and land management data was grouped into categories based on:

- soil pHH2O: (i) pH < 7.5 and (ii) pH > 7.5 (The soil pH values measured with CaCl2 were converted to

values measured in distilled water using a method described by Minasny et al. (2011));

- soil texture: (i) coarse (sandy loam, sandy clay loam, loamy sand), (ii) medium (clay loam, loam, silty

clay loam, silt, silt loam), and (iii) fine (clay, silt clay, sandy clay) (USDA, 1999);

- topsoil organic C concentration: low (<10 g C kg-1 soil), medium (10–20 g C kg-1 soil), and high (>20 g C

kg-1 soil);

- water input and management: (i) rain-fed and annual precipitation <450 mm, (ii) rain-fed and annual

precipitation >450 mm, (iii) sprinklers, (iv) flooded, (v) furrow or surface irrigation, and (vi) drip

irrigation;

- type of N fertilizer: (i) synthetic (including all types of mineral fertilizers), (ii) organic-solid (compost,

solid fraction of manures, solid organic residues), (iii) organic-liquid (pig/cattle slurries, liquid fraction

of slurries, digestates), (iv) organic-synthetic mixture, and (v) inhibitors (nitrification and/or urease

inhibitors: DCD, DMPP,NBPT);

- N fertilizer rate: (i) <100 kg N ha-1, (ii) 100–400 kg N ha-1, and (iii) >400 kg N ha-1;

- type of crop: (i) winter cereals (hereafter: ‘cereals’), (ii) horticulture, (iii) maize, (iv) rice, (v) perennials,

and (vi) other.

2.3. Calculation of emission factors

Most studies included in the meta-analysis did not explicitly report EFs since they were designed with different

aims. We calculated EFs as the difference between N2O emissions from a fertilized treatment (kg N2O N ha-1)

and the non-fertilized (control) treatment (kg N2O N-N ha-1) divided by applied N fertilizer (kg N ha-1). In 39% of

cases, there was no control treatment and these missing data were obtained through multiple imputation by

chained equations (Azur et al., 2011) with IBM SPSS Statistics 24 (for a detailed description of missing data

treatment and sensitivity tests see Supplementary material 2).

2.4. Data analysis

We performed a standard pair-wise meta-analysis using emission factors (EFs) as effect sizes with MetaWin

version 2 (Rosenberg et al., 2000). Mean effect sizes for each grouping and the 95% confidence intervals (CI)

generated by bootstrapping (999 iterations) were calculated using a categorical random effects model (Adams

et al., 1997). For a detailed description of the statistical procedure see Supplementary material 2. Mean effect

sizes were considered significantly different from each other if their 95% CI did not overlap; they were

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considered significantly different from the default IPCC Tier I value (1%) if the 95% CIs did not overlap with 1%.

To test the possibility of publication bias (studies showing no significant effects might not be published), the

Rosenthal's fail-safe N test was used (Rosenthal, 1979).

2.5. Case study: effect of EF choice on Spanish N2O emissions estimation

We chose Spain to examine the effect of applying the EFs found in this study because Spain includes both rain-

fed and irrigated crops, and has one of the largest agricultural land uses within Europe. In addition, nutrient

budgets at the regional scale have been well developed for Spain (Lassaletta et al., 2014; Sanz-Cobena et al.,

2014b). We processed the information provided by MMARM (2010) on N fertilizer use (organic and synthetic)

for rain-fed and irrigated crops (by surface) in Spanish NUTS3 (Nomenclature of territorial Units for statistics,

level 3) regions to estimate the total input of fertilizer per climatic region (temperate and Mediterranean) and

water management type. We then compared two methods to calculate the Spanish national N2O emissions: 1)

‘Current EF’, we applied an EF = 1.0% (IPCC, 2006) on the N inputs; 2) ‘New EFs’, the EFs obtained in this study

for rain-fed, furrow, sprinkler and drip-irrigated systems in Mediterranean areas, and the IPCC (2006) EF for

temperate areas in the cropping systems of northern Spain.

3. Results

3.1. Cumulative N2O emissions and EF for Mediterranean regions

A total of 53 field studies analyzing N2O emissions in Mediterranean areas have been published in the last 10

years from four of the five Mediterranean regions worldwide (see Supplementary material 2 for regional

description). The cumulative emissions compiled here ranged from 0.15 kg N2O N ha-1 in a rice crop in

California (Simmonds et al., 2015) to 43.3 kg N2O N ha-1 in a maize field in Israel (Heller et al., 2010), with a

mean value of 2.8 kg N2O N ha-1. N2O emissions were on average largest for drip irrigation (4.6 kg N2O N ha-1)

and smallest for flooded irrigation (0.5 kg N2O N ha-1) systems (Table 2). Synthetic fertilizers were the

dominant type of fertilizer in all irrigation systems (Fig. S2) with drip irrigation systems receiving the most N

fertilizer (295 kg N ha-1), with some cases of extremely high (1500 kg N ha-1) application rates (Heller et al.,

2010). Treatments with a mixture of organic-synthetic fertilizers emitted the most N2O (9.8 kg N2O N ha-1),

which is related to the high average N application rate in this group (535 kg N ha-1). Organic-liquid fertilizers

were applied at similar rates as synthetic fertilizers, but their emissions were on average higher (4.8 vs. 1.7 kg

N2O N ha-1). The use of organic-solid fertilizers or the addition of inhibitors led to the lowest average

cumulative emissions (1.8 and 1.2 kg N2O N ha-1, respectively) (Table 2). Maize and horticulture crops had the

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highest N2O emissions (4.7 and 3.4 kg N2O N ha-1), while rice and cereal crops had the lowest (0.5 and 0.7 kg

N2O N ha-1) (Table 2).

Table 2 The number of observations (N), mean and standard deviation (SD) of cumulative N2O emissions, N application rate and experiment duration for some of the factors with a significant influence on N2O emissions from agricultural fields.

Water Cumulative N2O emissions (kg N2O N ha-1)

N application rate (kg N ha-1)

Experiment duration (days)

N Mean SD Mean SD Mean SD

Water Drip 55 4.6 9.5 295 387 299 110 Flooded 14 0.5 0.8 161 59 277 106 Furrow 29 2.9 4.7 205 94 254 92 Sprinkler 55 3.7 3.3 226 75 186 99 Rain-fed <450 mm 39 0.4 0.3 117 58 269 66 Rain-fed >450 mm 40 2.3 4.8 153 125 253 131

Fertilizer type Organic-liquid 30 4.8 5.4 172 95 251 71 Organic-solid 26 1.8 2.3 238 155 227 114 Mixture 22 9.8 13.5 535 523 327 73 Synthetic 131 1.7 3.1 157 77 260 108 Inhibitora 23 1.2 1.7 167 78 167 129

Crop type Maize 56 4.7 7.0 323 298 223 129 Horticulture 36 3.4 4.6 182 67 231 125 Perennial 22 1.2 1.5 104 73 297 100 Cereal 61 0.7 0.6 138 62 277 68 Rice 14 0.5 0.8 161 59 277 106 Others 43 4.5 8.8 230 290 243 112

ainhibitor refers to treatments with synthetic and/or organic fertilizers where nitrification or urease inhibitors were

applied.

The mean EF for Mediterranean crops (EFMed)—covering rain-fed and irrigated systems, arable and permanent

crops, organically and synthetically fertilized systems (treatments with inhibitors excluded) for all

Mediterranean-type climate areas was 0.50% 0.12 (EFMed 95%CI, N = 200; Rosenthal’s fail-safe test: 4830).

Grouping into different categories allowed us to identify which factors (soil, crop, irrigation system, type of

fertilizer and application rate) had a significant impact on averaged EFs, providing key information when

proposing N2O mitigation strategies.

3.2. Influence of soil characteristics on EF

Soil pH, soil organic C or soil texture did not significantly affect EFs. Soil pHs ranged from 4.8 in a rice

experimental station field site in California (Simmonds et al., 2015) to 8.5 in a cereal crop in north-eastern

Spain (Plaza-Bonilla et al., 2014), with most soils having a neutral to alkaline pH (in 83% of the cases, pH > 7).

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The concentration of organic C in soils ranged from 4 g C kg-1 soil in California (Schellenberg et al., 2012) to 133

g C kg-1 soil in Chile (Vistoso et al., 2012), and the average soil organic C concentration was 15.9 g C kg-1 soil.

EFs did not significantly differ among soils with low (EF: 0.56, N = 59), medium (EF: 0.51, N = 94) or high (EF:

0.37, N = 5) organic C concentrations. Finally, soil texture had no significant effect on average EFs, although

trends suggested that larger EFs could be expected from coarse (EF: 0.58%, N = 77) and medium-textured soils

(EF: 0.48%, N = 100), than from fine-textured soils (EF: 0.27%, N = 22).

3.3. Influence of water management on EF

Rain-fed systems had an average EF of 0.27% 0.21 (N = 62) which was significantly lower than 1% (Fig. 2).

Studies under dry Mediterranean conditions (average annual precipitation <450 mm) had lower EFs (EF: 0.21%

0.26, N = 38) than studies in areas with an average annual precipitation >450 mm (EF: 0.32% 0.33, N = 24).

There was high variability in EFs between types of irrigation management (Fig. 2). Drip-irrigated (including both

surface and subsurface) and furrow systems had lower EFs (EF: 0.51% 0.26, N = 52 and EF: 0.47% 0.36, N = 27,

respectively) than sprinklers (EF: 0.91% 0.24, N = 45), which was close and not significantly differ from the IPCC

default EF.

It is important to note that drip-irrigated systems had the highest level of N fertilization (Table 2), which could

have biased the results of the meta-analysis, increasing the EF for this group. Flooded systems (rice fields) had

the lowest EF (0.19% 0.50, N = 14), in line with IPCC (2006) guidelines.

3.4. Influence of fertilizer type and application rate on EF

The highest EFs corresponded with organic-liquid fertilizers (EF: 0.85% 0.30, N = 30), which were mostly pig or

cattle slurries, or the liquid fraction of their digestates (Fig. 3); this EF did not significantly differ from 1%. The

rest of the fertilizer types had an EF significantly lower than 1% but were statistically similar to each other. The

use of nitrification/urease inhibitors decreased the average EFs (EF: 0.14% 0.32, N = 23) when compared with

synthetic, organic-liquid, and mixtures of organic and synthetic fertilizers, but was similar to EFs from organic-

solid fertilizers (EF: 0.19% 0.33, N = 24). Crops fertilized with organic-solid fertilizers received, on average,

almost double the amount of N than those with synthetic or liquid fertilizers (Table 2), which reinforces

organic-solid fertilization as a strategy to decrease EFs. Although not statistically significant, higher N

application rates increased EFs. Low N application rates (<100 kg N ha-1) had the lowest EFs (EF: 0.27%, N = 40),

whereas high N application rates (>400 kg N ha-1) resulted in EFs that did not significantly differ from the 1%

IPCC value (EF: 0.82%, N = 15).

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Fig. 2. The influence of different irrigation options on changes in N2O emission factors (EFs) in Mediterranean-type climate areas. Symbols represent mean effect sizes [EFs (%)] with 95% confidence intervals. The numbers shown in parentheses correspond to observations in each class upon which the statistical analysis was based. For this analysis, treatments with nitrification inhibitors were excluded (see Methods).

Fig. 3. The impact of the type of N fertilizer and application rate on changes in N2O emission factors (EFs) in Mediterranean-type climate areas. Symbols represent mean effect sizes [EFs (%)] with 95% confidence intervals. The numbers shown in parentheses correspond to observations in each class upon which the statistical analysis was based.

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3.5. Influence of crop types on EF

Five out of the six considered crops presented EFs significantly lower than 1% (Fig. 4). Rice and cereals (wheat,

barley, and oat) had the smallest EFs (EF: 0.19% 0.51, N = 14 for rice and 0.26% 0.22, N = 53 for cereals).

Perennials (including vineyards, almonds, and olive orchards) and others (including pasture, legumes,

rapeseed, crop rotations and bare soil) had intermediate EFs (EF: 0.54%, N = 19 for perennials and EF: 0.47%, N

= 33 for others). Horticultural crops (melons, onions, tomatoes, and potatoes) showed a slightly higher than

average EF (EF: 0.63% 0.31, N = 34). Finally, maize had a relatively high average EF (EF: 0.83% 0.26, N = 47)

which did not significantly differ from the 1% default.

3.6. Case study: effect of EF choice on Spanish N2O emissions estimation

Table 3 shows ‘current EF’ used by national inventories (IPCC, 2006) and the ‘New EFs’ determined from this

study for rain-fed, furrow, sprinkler and drip-irrigated systems in Mediterranean crops. Nitrous oxide emissions

from Spanish agriculture vary considerably depending on the calculation method. The emissions from

Mediterranean Spanish agriculture calculated with the current EF (12.5 Gg N2O N yr-1) exceeded the value

using the new EFs (5.5 Gg N2O N yr-1) by a factor of two and this had a substantial impact on the estimates of

total national emissions from cropping systems (Table 4).

Fig. 4. Average N2O emission factors (EFs) in Mediterranean-type climate areas depending on the type of crop. Symbols represent mean effect sizes [EFs (%)] with 95% confidence intervals. The numbers shown in parentheses correspond to observations in each class upon which the statistical analysis was based. For this analysis, treatments with nitrification inhibitors were excluded (see Methods).

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Table 3 Emission factors (EFs) used to estimate total N2O emissions in the Spanish cropping systems: current EFs according to IPCC (2006) and the new values for Mediterranean areas developed in this work for different irrigation systems. The percentages in brackets show the proportion of the area under each irrigation system in Spain.

EFs Temperate climate Mediterranean climate

Current Rain-fed crops 1.0% 1.0% Irrigated crops 1.0% 1.0%

New EFs Rain-fed crops 1.0% 0.27% Irrigated furrow (27% surface) 1.0% 0.47% Sprinkler (24% surface) 1.0% 0.91% Drip (49% surface) 1.0% 0.51%

Table 4 Comparison of total N2O emissions in Spanish cropping systems (MMARM, 2010) after the application of the current EFs and the new EFs obtained in this study, considering that all the irrigated crops are furrow, sprinkler or drip irrigated. The percentages in brackets show the proportion of the area under each irrigation system in Spain.

Temperate climate Mediterranean climate Total Fertilizer N input (synth + org) Rain-fed crops 137 585 722 (Gg N yr-1) Irrigated crops 13 664 678 Total 151 1249 1400

Current EFs Rain-fed crops 1.4 5.8 7.2 Total N2O emissions Irrigated crops 0.1 6.6 6.8 (Gg N yr-1) Total 1.5 12.5 14.0

Rain-fed crops 1.4 1.6 3.0 New EFs Furrow (27%) 0.0 0.8 0.9 Total N2O emissions Sprinkler (24%) 0.0 1.5 1.5 (Gg N yr-1) Drip (49%) 0.1 1.7 1.7 Total 1.5 5.5 7.0

4. Discussion

In this paper, we derived an EF for N2O emissions from Mediterranean regions (EFMed: 0.5%) and

demonstrated that EFs in Mediterranean-cultivated lands are significantly lower than the 1% IPCC Tier I

default value (IPCC, 2006) or the 1.25% (IPCC, 1996) used to calculate N2O emissions in response to

applying N fertilizer to land. We, therefore, recommend that Mediterranean countries, or regions, consider

refining their national inventories to reflect the relatively small EF. Here, we show the implications of such a

change by using the EFs obtained in this study to estimate total N2O emissions from cropping systems in

Spain and compare them to estimates using the IPCC default value.

To derive statistically robust estimates of EFs, we opted to retain studies without control measurements.

We performed a sensitivity test (see Supplementary material 2) which demonstrated that including these

studies had no impact on the mean EFMed (EF: 0.496% including all studies and EF: 0.463% excluding cases

without control, see Supplementary material 2). We, therefore, conclude that the EFMed is robust, but due

to the high heterogeneity of the studies included in the dataset, it was often difficult to find significant

differences between different management strategies. Further field research, measuring emissions over

13

the whole year and including control treatments, is merited to better quantify EFs for the various

management options in Mediterranean systems.

4.1. Influence of soil characteristics on EF

Soil characteristics show very limited impact of EFs. This finding seems to contradict previous studies where

soil organic C concentration and pH had a clear impact on denitrification and therefore N2O emissions (Li et

al., 2005; Šimek and Cooper, 2002). However, these relationships might be difficult to find in our dataset,

where most soils had a neutral or slightly alkaline pH and similar (in general low) concentrations of organic

C, with other variables having a stronger effect on N2O emissions (N application rate, soil water content,

type of fertilizer applied, etc.). In addition, although denitrification is generally identified as the major

process generating N2O in most cropping systems, this does not necessarily stand for studies under

Mediterranean conditions, where the importance of nitrifier-nitrification and nitrifier-denitrification have

been documented (Sánchez-García et al., 2014; Sánchez-Martín et al., 2008). Nitrification (contrarily to

denitrification) does not need an additional source of C and therefore if nitrification pathways dominate,

the soil C availability may not play an important role on N2O emissions.

Although not significant, we found higher EFs in coarse/ medium-textured soils (EF: 0.58 and 0.48%) than in

fine-textured soils (EF: 0.27%). Since denitrification needs anaerobic conditions, which are more likely to

occur in fine-textured soils, this result seems contradictory. Our finding might be related to (i) complete

denitrification (transformation to N2) in less-aerated fine-textured soils (Šimek and Cooper, 2002) or (ii)

nitrification processes having an important role in N2O emissions, with higher nitrification rates in low

water content, well-aerated soils (Thomsen et al., 2003). Also, previous studies found higher annual

denitrification losses in loamy soils than sandy or clay-textured soils, which was interpreted as a limitation

of C diffusion by adsorption to clays in fine-textured soils (Barton et al., 1999).

4.2. Influence of water management on EF

Among the irrigation technologies used in Mediterranean cropping systems, furrows are still widespread in

summer-irrigated crops and sprinkler irrigation systems are on the increase in Spain (MAGRAMA, 2014).

However, since many Mediterranean regions suffer from water scarcity, water-saving irrigation systems

such as drip irrigation (both surface and subsurface) are being developed. The area sown to maize under

drip irrigation is expected to increase due to higher water use efficiency, maintained crop yields and

technical viability (Couto et al., 2013). Despite these advantages, the impact of drip irrigation systems on

N2O emissions is poorly documented.

14

Our analyses revealed that EFs for N2O from drip-irrigated systems are much lower than those in which

water is applied through sprinklers, even when the average N application rate was higher with drip

irrigation. This is consistent with other field-based research (Kallenbach et al., 2010; Sánchez-Martín et al.,

2008) and a previous review under Mediterranean conditions (Aguilera et al., 2013a). The reduction in N2O

emissions with drip irrigation is probably caused by a reduction in the rate of water application compared

with other conventional systems (Sharma-sarkar et al., 2001). This may decrease the soil-water-filled pore

space (WFPS) below the optimum range for N2O production through denitrification, which is 60–90%

depending on soil type (Barton et al., 1999,Sanz-Cobena et al., 2014a). WFPS levels below this threshold are

common in many of the drip irrigation studies included in this review. For instance, in Abalos et al. (2014),

the WFPS was below 65% for 84% of the experimental period; it never exceeded 50% in the study of

Schellenberg et al. (2012), and it ranged from 20 to 30% and 40–60% in Kallenbach et al. (2010) and

Kennedy et al. (2013), respectively. Therefore, our results suggest that drip irrigation represents an

effective N2O mitigation practice in Mediterranean irrigated systems. These benefits, however, should be

evaluated together with other effects on the GHG balance and further socioenvironmental consequences.

For example, increased infrastructure material requirements and energy needs for pressurizing the

irrigation water might offset drip irrigation N2O-related emission savings in certain situations, while

reduced water use (and related energy consumption) might be the main component responsible for

emission reduction in other situations (Sanz-Cobena et al., 2017).

The lower EFs found under furrow irrigation compared to sprinkler irrigation might be related to a slightly

lower average N application in the furrow systems included in our dataset and to a different soil wetting

pattern, favoring complete denitrification to N2 after irrigation events in furrows (Sánchez-Martín et al.,

2008).

Our results show that rain-fed crops with less than 450 mm rainfall and flooded systems have the lowest

EFs of all systems (Fig. 2). In contrast, rain-fed crops in areas with annual precipitation greater than 450 mm

have larger emissions. These findings show the strong effect of specific climatic conditions and soil

moisture on the performance of Mediterranean cropping systems in terms of N2O emissions. The

distribution of rain inputs also plays a relevant role. The first rainfall after long periods of drought (common

in summers of Mediterranean areas) usually triggers N2O emissions. This pulsing effect, also observed in the

dry areas of drip-irrigated crops, is due to the accumulation of mineral N in dry soils and the reactivation of

water-stressed bacteria after rainfall events (Sánchez-Martín et al., 2010a; Skiba et al., 1997).

Drip irrigation may have an adverse side-effect as its use has been associated with enhanced emissions of

nitric oxide (NO) (Abalos et al., 2014). This is because the lower WFPS may favor NO production from

15

nitrification. Pilegaard (2013) reported maximum NO emissions at intermediate soil moisture (40–60%

WFPS) since NO is highly reactive and will be consumed at higher soil moisture.

4.3. Influence of fertilizer type and application rate on EF

Our results suggest that the use of liquid manures and inorganic N fertilizers results in greater N2O

emissions than organic-solid fertilizers such as composted manures and green wastes. Liquid and inorganic

N fertilizers are likely to be more readily available to plants and microorganisms, whereas solid organically-

bound N requires decomposition and microbial mineralization to be used in N2O-producing processes

(Poodle et al., 2002). Composted organic fertilizer N is thus released more slowly, ultimately increasing N

uptake by crops (Ryals et al., 2015) and decreasing the potential for N2O emissions. It is notable that not all

organic fertilizers are equivalent with regard to their potential effects on N2O emissions. For example, fresh

manures and manure slurries can result in relatively large N2O emissions. A recent meta-analysis found the

IPCC Tier II model underestimated N2O emissions from cattle manure in the United States by an order of

magnitude (Owen and Silver, 2015). Davidson (2009) also suggested that manure management was a

dominant source of atmospheric N2O concentrations, accounting for more than 40% of anthropogenic N2O

emissions. Liquid manures are rich in both N and C, potentially facilitating N2O production in low C

environments, mostly through denitrification. As already observed in Aguilera et al. (2013a), solid manure

would result in lower N2O emissions, unlike in more humid areas with relatively high decomposition rates

and N2O EFs (Owen et al., 2015).

As expected, nitrification/urease inhibitors effectively reduced EFs from Mediterranean systems (Mosier et

al., 1996). In a recent review, Gilsanz et al. (2016) developed EFs of 0.42% 2.2 and 0.70% 3.3 for DCD and

DMPP, respectively, two commonly used nitrification inhibitors. The lower EF found in our study (0.14%

0.32) agrees with the low baseline EFs found in the studies included in our dataset. Thus, inhibitors seem to

be a good strategy to mitigate direct N2O emissions under Mediterranean conditions, although the

potential is lowered by the relatively small baseline emissions in Mediterranean systems.

In agreement with previous studies (Kim et al., 2013; Shcherbak et al., 2014), increasing fertilizer

application rates led to increased EFs. We found that applying N fertilizers over 400 kg N ha-1 resulted in EFs

that did not significantly differ from the 1% IPCC Tier I default value. The lack of statistical significance

between N doses is probably related to the fact that in our dataset most studies only considered one N

application rate, with a limited number of cases with very low or high N fertilization rates.

16

4.4. Influence of crop types on EF

In a previous quantitative review of Mediterranean cropping systems, Aguilera et al. (2013a) observed that

the differences in cumulative N2O emissions among crop types clearly respond to the management

characteristics of each crop type; our results confirm these conclusions. Generally, the crop types in which

water and fertilizer applications are low (see Figs. S3 and S4 and Table 2), such as rain-fed crops (winter

cereals), have the lowest N2O response to N applications. A low EF for rice is associated with flooding which

generates anaerobic conditions favoring complete denitrification to N2, thereby reducing N2O release from

the soil (Conrad, 1996). Maize has a high EF, possibly because it is irrigated without implementation of

water-saving techniques and has on average higher N application rates. The wide confidence intervals

observed for the EFs in perennials and rice are due to the lower number of observations within these crop

categories.

4.5. Case study: effect of EF choice on Spanish N2O emissions estimation

In this work we have seen how the application of EFs adapted to Mediterranean conditions can significantly

reduce the national estimates of total N2O emissions from cropping systems. Applying the new EFs has

consequences for determining the effectiveness of N2O mitigation strategies in Mediterranean regions, as

baseline emissions will be smaller than those suggested by Tier I emission estimates. The level of indirect

emissions is, however, highly uncertain, and published information is scarce, and has thus not been

assessed in this study. IPCC Tier I proposes an EF for indirect emissions of 0.75% while Garnier et al. (2009,

2013) estimated that, for the Seine temperate basin, indirect emissions represented 13– 17% of total direct

emissions. Due to the regulation of water in Mediterranean agricultural areas in Spain through a dense

drainage network and reservoirs (Aguilera et al., 2015), the potential for denitrification could be high and

could, therefore, generate high indirect emissions. The magnitude of indirect N2O emissions in

Mediterranean areas is an interesting area for future research.

5. Concluding remarks

The average EF for nitrous oxide emissions in Mediterranean cropping systems was 50% lower than the

IPCC Tier I default value (1%), which is largely based on values observed in temperate regions. The most

important factors controlling the magnitude of soil N2O EFs from Mediterranean regions were water regime

(irrigation technique or precipitation amount) and fertilizer type and application rate. In rain-fed systems

with precipitation below 450 mm, the EF is much lower than the IPCC values. The EF for sprinkler-irrigated

systems is similar to that for temperate cropping systems, whereas drip-irrigated systems have a high

17

potential for mitigation (EF: 0.51%). The N fertilizer rate altered EFs, suggesting a non-linear relationship

between N2O emissions and N application rate. Intensive cropping systems, such as irrigated maize, tended

to have higher EFs than less intensive systems such as cereals.

Applying specific EFs would lower estimates of total N2O emissions in countries with large areas of

agricultural soils in Mediterranean climates. For example, applying current Tier I EFs to Spanish cropping

systems leads to a total N2O emission estimate that is a factor of two higher than when applying the new

EFs from our analysis (14 Gg N2O N yr-1 vs. 7 Gg N2O N yr-1). Our results indicate that N2O emissions from

Mediterranean agriculture are much lower than expected and that with the new EFs, the effect of

mitigation strategies such as drip irrigation or using nitrification inhibitors, even if highly significant, may be

smaller in absolute terms (since baseline emissions will be lower).

Acknowledgements

The authors are grateful to M. Scholes, D. Plaza-Bonilla, S. Menendez, P. Merino, S.C. Maris, H. Heller, D.

Savvas, C. K. Kontopoulou, who were contacted and kindly supplied any missing information necessary for

the meta-analysis. Special thanks to J.P.C. Eekhout for preparing Fig. 1 and F. Estellés for providing the basic

data for the calculation of the fertilization in Spain. Also thanks to two anonymous reviewers for their

helpful comments. M. L. Cayuela was supported by a ‘Ramon y Cajal’ research contract from the Spanish

Ministry of Economy and Competitiveness. Thanks to Fundación Séneca, Agencia Regional de Ciencia y

Tecnología de la Región de Murcia for support (grant number 19281/PI/14). Australian studies included in

the meta-analysis were funded by the Australian Government, the Grains Research and Development

Corporation, and the Department of Agriculture and Food WA.

Appendix A. Supplementary data

Supplementary data associated with this article can be found, in the online version, at

http://dx.doi.org/10.1016/j.agee.2016.10.006.

18

References

Abalos, D., Sanz-Cobena, A., Misselbrook, T., Vallejo, A., 2012. Effectiveness of urease inhibition on the

abatement of ammonia, nitrous oxide and nitric oxide emissions in a non-irrigated Mediterranean barley

field. Chemosphere 89, 310– 318.

Abalos, D., Sanz-Cobena, A., Garcia-Torres, L., van Groenigen, J., Vallejo, A., 2013. Role of maize stover

incorporation on nitrogen oxide emissions in a non-irrigated Mediterranean barley field. Plant Soil 364,

357–371.

Abalos, D., Sanchez-Martin, L., Garcia-Torres, L., van Groenigen, J.W., Vallejo, A., 2014. Management of

irrigation frequency and nitrogen fertilization to mitigate GHG and NO emissions from drip-fertigated crops.

Sci. Total Environ. 490, 880– 888.

Adams, D.C., Gurevitch, J., Rosenberg, S., 1997. Resampling tests for meta-analysis of ecological data.

Ecology 78, 1277–1283.

Aguilera, E., Lassaletta, L., Sanz-Cobena, A., Garnier, J., Vallejo, A., 2013a. The potential of organic fertilizers

and water management to reduce N2O emissions in Mediterranean climate cropping systems. A review.

Agric. Ecosyst. Environ. 164, 32–52.

Aguilera, E., Lassaletta, L., Gattinger, A., Gimeno, B.S., 2013b. Managing soil carbon for climate change

mitigation and adaptation in Mediterranean cropping systems: a meta-analysis. Agric. Ecosyst. Environ.

168, 25–36.

Aguilera, R., Marcé, R., Sabater, S., 2015. Detection and attribution of global change effects on river

nutrient dynamics in a large Mediterranean basin. Biogeosciences 12, 4085–4098.

Alluvione, F., Bertora, C., Zavattaro, L., Grignani, C., 2010. Nitrous oxide and carbon dioxide emissions

following green manure and compost fertilization in corn. Soil Sci. Soc. Am. J. 74, 384–395.

Alsina, M.M., Fanton-Borges, A.C., Smart, D.R., 2013. Spatiotemporal variation of event related N2O and

CH4 emissions during fertigation in a California almond orchard. Ecosphere 4, art1.

Andrews, S.S., Mitchell, J.P., Mancinelli, R., Karlen, D.L., Hartz, T.K., Horwath, W.R., Pettygrove, G.S., Scow,

K.M., Munk, D.S., 2002. On-farm assessment of soil quality in California's Central Valley. Agron. J. 94, 12–23.

19

Angst, T.E., Six, J., Reay, D.S., Sohi, S.P., 2014. Impact of pine chip biochar on trace greenhouse gas

emissions and soil nutrient dynamics in an annual ryegrass system in California. Agric. Ecosyst. Environ. 191,

17–26.

Aschmann, H., 1973. Distribution and peculiarity of Mediterranean ecosystems. In: Di Castri, F., Mooney,

H.A. (Eds.), Mediterranean-Type Ecosystems: Origin and Structure. Springer, New York, pp. 11–19.

Azur, M.J., Stuart, E.A., Frangakis, C., Leaf, P.J., 2011. Multiple imputation by chained equations: what is it

and how does it work? Int. J. Meth. Psychiatr. Res. 20, 40– 49.

Barton, L., Mclay, C.D.A., Schipper, L.A., Smith, C.T., 1999. Annual denitrification rates in agricultural and

forest soils: a review. Aus. J. Soil Res. 37, 1073–1093.

Barton, L., Kiese, R., Gatter, D., Butterbach-Bahl, K., Buck, R., Hinz, C., Murphy, D.V., 2008. Nitrous oxide

emissions from a cropped soil in a semi-arid climate. Glob. Change Biol. 14, 177–192.

Barton, L., Murphy, D.V., Kiese, R., Butterbach-Bahl, K., 2010. Soil nitrous oxide and methane fluxes are low

from a bioenergy crop (canola) grown in a semi-arid climate. Global Change Biol. 2, 1–15.

Barton, L., Murphy, D., Butterbach-Bahl, K., 2013. Influence of crop rotation and liming on greenhouse gas

emissions from a semi-arid soil. Agric. Ecosyst. Environ. 167, 23–32.

Bosco, S., Volpi, I., Nassi o Di Nasso, N., Triana, F., Roncucci, N., Tozzini, C., Villani, R., Laville, P., Neri, S.,

Mattei, F., Virgili, G., Nuvoli, S., Fabbrini, L., Bonari, E., 2015. LIFE + IPNOA mobile prototype for the

monitoring of soil N2O emissions from arable crops: first-year results on durum wheat. Ital. J. Agron. 10, 8.

Bouwman, A.F., Boumans, L.J.M., Batjes, N.H., 2002. Emissions of N2O and NO from fertilized fields:

summary of available measurement data. Glob. Biogeochem. Cy. 16 6-1–6-13.

Castaldi, S., Riondino, M., Baronti, S., Esposito, F.R., Marzaioli, R., Rutigliano, F.A., Vaccari, F.P., Miglietta, F.,

2011. Impact of biochar application to a Mediterranean wheat crop on soil microbial activity and

greenhouse gas fluxes. Chemosphere 85, 1464–1471.

Conrad, R., 1996. Soil microorganisms as controllers of atmospheric trace gases (H2, CO, CH 4, OCS, N2O, and

NO). Microbiol. Rev. 60, 609–640.

Couto, A., Padin, A.R., Reinoso, B., 2013. Comparative yield and water use efficiency of two maize hybrids

differing in maturity under solid set sprinkler and two different lateral spacing drip irrigation systems in

Leon, Spain. Agric. Water Manage. 124, 77–84.

20

Davidson, E.A., 2009. The contribution of manure and fertilizer nitrogen to atmospheric nitrous oxide since

1860. Nat. Geosci. 2, 659–662.

Garland, G.M., Suddick, E., Burger, M., Horwath, W.R., Six, J., 2011. Direct N2O emissions following

transition from conventional till to no-till in a cover cropped Mediterranean vineyard (Vitis vinifera). Agric.

Ecosyst. Environ. 141, 234–239.

Garland, G.M., Suddick, E., Burger, M., Horwath, W.R., Six, J., 2014. Direct N2O emissions from a

Mediterranean vineyard: event-related baseline measurements. Agric. Ecosyst. Environ. 195, 44–52.

Garnier, J., Billen, G., Vilain, G., Martinez, A., Silvestre, M., Mounier, E., Toche, F., 2009. Nitrous oxide (N2O)

in the Seine river and basin: observations and budgets. Agric. Ecosyst. Environ. 133, 223–233.

Garnier, J., Vilain, G., Jehanno, S., Silvestre, M., Billen, G., Poirier, D., Martinez, A., Decuq, C., Cellier, P.,

Abril, G., 2013. Methane emissions from land use, livestock farming, and the river network of the Seine

basin (France). Biogeochemistry 116, 199–214.

Gerber, J.S., Carlson, K.M., Makowski, D., Mueller, N.D., Garcia de Cortazar-Atauri, I., Havlík, P., Herrero, M.,

Launay, M., O'Connell, C.S., Smith, P., West, P.C., 2016. Spatially explicit estimates of N2O emissions from

croplands suggest climate mitigation opportunities from improved fertilizer management. Global Change

Biol. 22, 3383–3394. doi:http://dx.doi.org/10.1111/gcb.13341.

Gilsanz, C., Baez, D., Misselbrook, T.H., Dhanoa, M.S., Cardenas, L.M., 2016. Development of emission

factors and efficiency of two nitrification inhibitors, DCD and DMPP. Agric. Ecosyst. Environ. 216, 1–8.

Grigg, D.B., 1974. Mediterranean agriculture. In: Grigg, D.B. (Ed.), The Agricultural Systems of the World. An

Evolutionary Approach. Cambridge University Press, Cambridge, pp. 123–151.

Heller, H., Bar-Tal, A., Tamir, G., Bloom, P., Venterea, R.T., Chen, D., Zhang, Y., Clapp, C. E., Fine, P., 2010.

Effects of manure and cultivation on carbon dioxide and nitrous oxide emissions from a corn field under

Mediterranean conditions. J. Environ. Qual. 39, 437–448.

Huérfano, X., Fuertes-Mendizábal, T., Duñabeitia, M.K., González-Murua, C., Estavillo, J.M., Menéndez, S.,

2015. Splitting the application of 3,4-dimethylpyrazole phosphate (DMPP): Influence on greenhouse gases

emissions and wheat yield and quality under humid Mediterranean conditions. Eur. J. Agron. 64, 47–57.

21

Hube, S., Alfaro, M., Scheer, C., Brunk, C., Ramírez, L., Rowling, D., Grace, P., 2017. Effect of nitrification and

urease inhibitors on nitrous oxide and methane emissions from an oat crop in a volcanic ash soil. Agric.

Ecosyst. Environ. 238, 46–54.

IPCC, 1996. Revised 1996 IPCC Guidelines for National Greenhouse Gas Inventories. Available at:

http://www.ipcc-nggip.iges.or.jp/public/gl/invs1.html. (accessed 22.01.2016).

IPCC, 2006. 2006 IPCC Guidelines for National Greenhouse Gas Inventories. Ed: H.S. Eggleston, L. Buendia,

K. Miwa, T. Ngara and K. Tanabe (Hayama: Intergovernmental Panel on Climate Change, IGES). Available at:

http://www. ipcc-nggip.iges.or.jp/public/2006gl/index.html. (accessed 22.01.2016).

IPCC, 2016. Emission Factor Database. http://www.ipcc-nggip.iges.or.jp/EFDB/main.php. (accessed

03.03.2016).

Kallenbach, C.M., Rolston, D.E., Horwath, W.R., 2010. Cover cropping affects soil N2O and CO2 emissions

differently depending on type of irrigation. Agric. Ecosyst. Environ. 137, 251–260.

Kennedy, T.L., Suddick, E.C., Six, J., 2013. Reduced nitrous oxide emissions and increased yields in California

tomato cropping systems under drip irrigation and fertigation. Agric. Ecosyst. Environ. 170, 16–27.

Kim, D.G., Hernandez-Ramirez, G., Giltrap, D., 2013. Linear and nonlinear dependency of direct nitrous

oxide emissions on fertilizer nitrogen input: a meta-analysis. Agric. Ecosyst. Environ. 168, 53–65.

Kong, A.Y.Y., Fonte, S.J., van Kessel, C., Six, J., 2009. Transitioning from standard to minimum tillage Trade-

offs between soil organic matter stabilization, nitrous oxide emissions, and N availability in irrigated

cropping systems. Soil Tillage Res. 104, 256–262.

Kontopoulou, C.-K., Bilalis, D., Pappa, V.A., Rees, R.M., Savvas, D., 2015. Effects of organic farming practices

and salinity on yield and greenhouse gas emissions from a common bean crop. Sci. Hortic. Amsterdam 183,

48–57.

López-Fernández, S., Díez, J.A., Hernáiz, P., Arce, A., García-Torres, L., Vallejo, A., 2007. Effects of fertiliser

type and the presence or absence of plants on nitrous oxide emissions from irrigated soils. Nutr. Cycl.

Agroecosyst. 78, 279–289.

Lassaletta, L., Billen, G., Romero, E., Garnier, J., Aguilera, E., 2014. How changes in diet and trade patterns

have shaped the N cycle at the national scale: spain (1961– 2009). Reg. Environ. Change 14, 785–797.

22

Lee, J., Hopmans, J.W., van Kessel, C., King, A.P., Evatt, K.J., Louie, D., Rolston, D.E., Six, J., 2009. Tillage and

seasonal emissions of CO2: N2O and NO across a seed bed and at the field scale in a Mediterranean climate.

Agric. Ecosyst. Environ. 129, 378–390.

Leip, A., Busto, M., Winiwarter, W., 2011. Developing spatially stratified N2O emission factors for Europe.

Environ. Pollut. 159, 3223–3232.

Lesschen, J.P., Velthof, G.L., de Vries, W., Kros, J., 2011. Differentiation of nitrous oxide emission factors for

agricultural soils. Environ. Pollut. 159, 3215–3222.

Li, C., Frolking, S., Butterbach-Bahl, K., 2005. Carbon sequestration in arable soils is likely to increase nitrous

oxide emissions, offsetting reductions in climate radiative forcing. Clim. Change 72, 321–338.

Li, Y., Barton, L., Chen, D., 2011. Simulating response of N2O emissions to fertiliser N application and

climatic variability from a rain-fed and wheat cropped soil in Western Australia. J. Sci. Food Agric. 92, 1130–

1143.

MAGRAMA (Ministerio de Agricultura, Alimentación y Medio Ambiente), 2014. Inventario Nacional De

Emisiones De Contaminantes a La Atmósfera in Spanish. www.magrama.gob.es/es/calidad-y-evaluacion-

ambiental/temas/sistema-espanol-de-inventario-sei-/.

MMARM (Ministerion de Medioambiente, Rural y Marino), 2010. Balance del nitrógeno en la agricultura

española. Año 2008. Ministerio de Medio Ambiente, Rural y Marino, Madrid.

Maris, S.C., Teira-Esmatges, M.R., Arbonés, A., Rufat, J., 2015a. Effect of irrigation, nitrogen application, and

a nitrification inhibitor on nitrous oxide, carbon dioxide and methane emissions from an olive (Olea

europaea L.) orchard. Sci. Total Environ. 538, 966–978.

Maris, S.C., Teira-Esmatges, M.R., Català, M.M., 2015b. Influence of irrigation frequency on greenhouse

gases emission from a paddy soil. Paddy Water Environ. 14, 199–210.

Meijide, A., Díez, J.A., Sánchez-Martín, L., López-Fernández, S., Vallejo, A., 2007. Nitrogen oxide emissions

from an irrigated maize crop amended with treated pig slurries and composts in a Mediterranean climate.

Agric. Ecosyst. Environ. 121, 383–394.

Meijide, A., García-Torres, L., Arce, A., Vallejo, A., 2009. Nitrogen oxide emissions affected by organic

fertilization in a non-irrigated Mediterranean barley field. Agric. Ecosyst. Environ. 132, 106–115.

23

Minasny, B., McBratney, A.B., Brough, D.M., Jacquier, D., 2011. Models relating soil pH measurements in

water and calcium chloride that incorporate electrolyte concentration. Eur. J. Soil Sci. 62, 728–732.

Mosier, A.R., Parton, W.J., Valentine, D.W., Ojima, D.S., Schimel Delgado, J.A., 1996. CH4 and N2O fluxes in

the Colorado shortgrass steppe: 1. Impact of landscape and nitrogen addition. Glob. Biogeochem. Cy. 10,

387–399.

Olson, D.M., Dinerstein, E., Wikramanayake, E.D., Burgess, N.D., Powell, G.V.N., Underwood, E.C., D'Amico,

J.A., Strand, H.E., Morrison, J.C., Loucks, C.J., Allnutt, T. F., Lamoreux, J.F., Ricketts, T.H., Itoua, I., Wettengel,

W.W., Kura, Y., Hedao, P., Kassem, K., 2001. Terrestrial ecoregions of the world: a new map of life on Earth.

Bioscience 51, 933–938.

Owen, J., Silver, W.L., 2015. Greenhouse gas emissions from dairy manure management: a review of field-

based studies. Glob. Change Biol. 21, 550–565.

Owen, J., Parton, W.J., Silver, W.L., 2015. Long-term impacts of manure amendments on carbon and

greenhouse gas dynamics of rangelands. Glob. Change Biol. 21, 4533–4547.

Pereira, J., Figueiredo, N., Goufo, P., Carneiro, J., Morais, R., Carranca, C., Coutinho, J., Trindade, H., 2013.

Effects of elevated temperature and atmospheric carbon dioxide concentration on the emissions of

methane and nitrous oxide from Portuguese flooded rice fields. Atmos. Environ. 80, 464–471.

Philibert, A., Loyce, C., Makowski, D., 2012. Quantifying uncertainties in N2O emission due to N fertilizer

application in cultivated areas. PLoS One 7, e50950.

Pilegaard, K., 2013. Processes regulating nitric oxide emissions from soils. Philos. T. Roy. Soc. B 368,

20130126.

Pittelkow, C.M., Adviento-Borbe, M.A., Hill, J.E., Six, J., van Kessel, C., Linquist, B.A., 2013. Yield-scaled

global warming potential of annual nitrous oxide and methane emissions from continuously flooded rice in

response to nitrogen input. Agric. Ecosyst. Environ. 177, 10–20.

Plaza-Bonilla, D., Álvaro-Fuentes, J., Arrúe, J.L., Cantero-Martínez, C., 2014. Tillage and nitrogen fertilization

effects on nitrous oxide yield-scaled emissions in a rainfed Mediterranean area. Agric. Ecosyst. Environ.

189, 43–52.

24

Poodle, D.D., Horwath, W.R., Lanini, W.T., Temple, S.R., van Brugge, A.H.C., 2002. Comparison of soil N

availability and leaching potential crop yields and weeds in organic, low-input and conventional farming

systems in northern California. Agric. Ecosyst. Environ. 90, 125–137.

Ranucci, S., Bertolini, T., Vitale, L., Di Tommasi, P., Ottaiano, L., Oliva, M., Amato, U., Fierro, A., Magliulo, V.,

2011. The influence of management and environmental variables on soil N2O emissions in a crop system in

Southern Italy. Plant Soil 343, 83–96.

Rees, R.M., Augustin, J., Alberti, G., Ball, B.C., Boeckx, P., Cantarel, A., Castaldi, S., Chirinda, N., Chojnicki, B.,

Giebels, M., Gordon, H., Grosz, B., Horvath, L., Juszczak, R., Kasimir Klemedtsson, Å., Klemedtsson, L.,

Medinets, S., Machon, A., Mapanda, F., Nyamangara, J., Olesen, J.E., Reay, D.S., Sanchez, L., Sanz Cobena,

A., Smith, K.A., Sowerby, A., Sommer, M., Soussana, J.F., Stenberg, M., Topp, C.F.E., van Cleemput, O.,

Vallejo, A., Watson, C.A., Wuta, M., 2013. Nitrous oxide emissions from European agriculture; an analysis of

variability and drivers of emissions from field experiments. Biogeosciences 10, 2671–2682.

Rosenberg, M.S., Adams, D.C., Gurevitch, J., 2000. MetaWin: Statistical Software for Meta-Analysis. Version

2.0. Sinauer Associates, Sunderland, Massachusetts.

Rosenthal, R., 1979. The file drawer problem and tolerance for null results. Psychol. Bull. 86, 638–641.

Ryals, R., Hartman, M., Parton, W.J., DeLonge, M., Silver, W.S., 2015. Long-term climate change mitigation

potential with organic matter management on grasslands. Ecol. Appl. 25, 531–545.

Sánchez-García, M., Roig, A., Sánchez-Monedero, M.A., Cayuela, M.L., 2014. Biochar increases N2O

emissions under nitrification mediated pathways. Front. Env. Sci. 2

doi:http://dx.doi.org/10.3389/fenvs.2014.00025.

Sánchez-García, M., Sánchez-Monedero, M.A., Roig, A., López-Cano, I., Moreno, B., Benitez, E., Cayuela,

M.L., 2016. Compost vs. biochar amendment: a two-year field study evaluating soil C build-up and N

dynamics in an organically managed olive crop. Plant Soil doi:http://dx.doi.org/10.1007/s11104-016-2794-4

(in press).

Sánchez-Martín, L., Arce, A., Benito, A., Garcia-Torres, L., Vallejo, A., 2008. Influence of drip and furrow

irrigation systems on nitrogen oxide emissions from a horticultural crop. Soil Biol. Biochem. 40, 1698–1706.

Sánchez-Martín, L., Meijide, A., Garcia-Torres, L., Vallejo, A., 2010a. Combination of drip irrigation and

organic fertilizer for mitigating emissions of nitrogen oxides in semiarid climate. Agric. Ecosyst. Environ.

137, 99–107.

25

Sánchez-Martín, L., Sanz-Cobena, A., Meijide, A., Quemada, M., Vallejo, A., 2010b. The importance of the

fallow period for N2O and CH4 fluxes and nitrate leaching in a Mediterranean irrigated agroecosystem. Eur.

J. Soil Sci. 61, 710–720.

Sanz-Cobena, A., Sanchez-Martín, L., García, L., Vallejo, A., 2012. Gaseous emissions of N2O and NO and NO3

leaching from urea applied with urease and nitrification inhibitors to a maize (Zea mays) crop. Agric.

Ecosyst. Environ. 149, 64–73.

Sanz-Cobena, A., Abalos, D., Sánchez-Martin, L., Meijide, A., Vallejo, A., 2014a. Soil moisture content

determines the effect of the urease inhibitor NBPT on N2O emissions. Mitig. Adapt. Strategies Glob. Change

. http://link.springer.com/ article/10.1007/s11027-014-9548-5.

Sanz-Cobena, A., Lassaletta, L., Estellés, F., Prado, A.D., Guardia, G., Abalos, D., Aguilera, E., Pardo, G.,

Vallejo, A., Sutton, M.A., Garnier, J., Billen, G., 2014b. Yield-scaled mitigation of ammonia emission from N

fertilization: the Spanish case. Environ. Res. Lett. 9, 125005.

Sanz-Cobena, A., Lassaletta, L., Aguilera, E., del Prado, A., Garnier, J., Billen, G., Iglesias, A., Sánchez, B.,

Guardia, G., Abalos, D., Plaza-Bonilla, D., Puigdueta, I., Moral, R., Galán, E., Arriaga, H., Merino, P., Infante-

Amate, J., Meijide, A., Pardo, G., Alvaro-Fuentes, J., Gilsanz, C., Báez, D., Doltra, J., González, S., Cayuela,

M.L., Menendez, S., Diaz-Pines, E., Le-Noe, J., Quemada, M., Estellés, F., Calvet, S., van Grinsven, H., Yáñez,

D., Westhoek, H., Sanz, M.J., Sánchez-Jimeno, B., Vallejo, A., Smith, P., 2017. Strategies for greenhouse gas

emissions mitigation in Mediterranean agriculture: A review. Agric. Ecosyst. Environ. 238, 5–24.

Schellenberg, D.L., Alsina, M.M., Muhammad, S., Stockert, C.M., Wolff, M.W., Sanden, B.L., Brown, P.H.,

Smart, D.R., 2012. Yield-scaled global warming potential from N2O emissions and CH4 oxidation for almond

(Prunus dulcis) irrigated with nitrogen fertilizers on arid land. Agric. Ecosyst. Environ. 155, 7–15.

Schouten, S., van Groenigen, J.W., Oenema, O., Cayuela, M.L., 2012. Bioenergy from cattle manure?

Implications of anaerobic digestion and subsequent pyrolysis for carbon and nitrogen dynamics in soil. GCB

Bioenergy 4, 751–760.

Sharmasarkar, F.C., Sharmasarkar, S., Miller, S.D., Vance, G.F., Zhang, R., 2001. Assessment of drip and flood

irrigation on water and fertilizer use efficiencies for sugar beets. Agric. Water Manage. 46, 241–251.

Shcherbak, I., Millar, N., Robertson, G.P., 2014. Global metaanalysis of the nonlinear response of soil

nitrous oxide (N2O) emissions to fertilizer nitrogen. Proc. Natl. Acad. Sci. USA 111, 9199–9204.

26

Šimek, M., Cooper, J.E., 2002. The influence of soil pH on denitrification: progress towards the

understanding of this interaction over the last 50 years. Eur. J. Soil Sci. 53, 345–354.

Simmonds, M.B., Anders, M., Adviento-Borbe, M.A., van Kessel, C., McClung, A., Linquist, B.A., 2015.

Seasonal methane and nitrous oxide emissions of several rice cultivars in direct-seeded systems. J. Environ.

Qual. 44, 103–114.

Skiba, U., Fowler, D., Smith, K.A., 1997. Nitric oxide emissions from agricultural soils in temperate and

tropical climates: sources, controls and mitigation options. Nutr. Cycl. Agroecosyst. 48, 139–153.

Smith, P., Martino, D., Cai, Z., Gwary, D., Janzen, H., Kumar, P., McCarl, B., Ogle, S., O'Mara, F., Rice, C.,

Scholes, B., Sirotenko, O., Howden, M., McAllister, T., Pan, G., Romanenkov, V., Schneider, U., Towprayoon,

S., Wattenbach, M., Smith, J., 2008. Greenhouse gas mitigation in agriculture. Philos. Trans. R. Soc. B 363,

789–813.

Stehfest, E., Bouwman, L., 2006. N2O and NO emission from agricultural fields and soils under natural

vegetation: summarizing available measurement data and modeling of global annual emissions. Nutr. Cycl.

Agroecosyst. 74, 207–228.

Suddick, E.C., Six, J., 2013. An estimation of annual nitrous oxide emissions and soil quality following the

amendment of high temperature walnut shell biochar and compost to a small scale vegetable crop rotation.

Sci. Total Environ. 465, 298–307.

Tellez-Rio, A., García-Marco, S., Navas, M., López-Solanilla, E., Tenorio, J.L., Vallejo, A., 2015. N2O and CH4

emissions from a fallow?wheat rotation with low N input in conservation and conventional tillage under a

Mediterranean agroecosystem. Sci. Total Environ. 508, 85–94.

Tenuta, M., Sparling, B., 2011. A laboratory study of soil conditions affecting emissions of nitrous oxide

from packed cores subjected to freezing and thawing. Can. J. Soil Sci. 91, 223–233.

Thomsen, I.K., Schjønning, P., Olesen, J.E., Christensen, B.T., 2003. C and N turnover in structurally intact

soils of different texture. Soil Biol. Biochem. 35, 765–774.

Townsend-Small, A., Pataki, D.E., Czimczik, C.I., Tyler, S.C., 2011. Nitrous oxide emissions and isotopic

composition in urban and agricultural systems in southern California. J. Geophys. Res. 116, G01013.

USDA, 1999. Soil Taxonomy: A Basic System of Soil Classification for Making and Interpreting Soil Surveys.

US Government printing Office, Washington DC.

27

Vallejo, A., García-Torres, L., Díez, J.A., Arce, A., López-Fernández, S., 2005. Comparison of N losses (NO3 ,

N2O, NO) from surface applied, injected or amended (DCD) pig slurry of an irrigated soil in a Mediterranean

climate. Plant Soil 272, 313–325.

Vallejo, A., Skiba, U.M., García-Torres, L., Arce, A., López-Fernández, S., Sánchez-Martín, L., 2006. Nitrogen

oxides emission from soils bearing a potato crop as influenced by fertilization with treated pig slurries and

composts. Soil Biol. Biochem. 38, 2782–2793.

Vallejo, A., Meijide, A., Boeckx, P., Arce, A., García-Torres, L., Aguado, P.L., Sanchez-Martin, L., 2014. Nitrous

oxide and methane emissions from a surface drip-irrigated system combined with fertilizer management.

Eur. J. Soil Sci. 65, 386– 395.

Verheye, W., de la Rosa, D., 2005. Mediterranean Soils, in Land Use and Land Cover, from Encyclopedia of

Life Support Systems (EOLSS), Developed Under the Auspices of the UNESCO. Eolss Publishers, Oxford, UK.

Verhoeven, E., Six, J., 2014. Biochar does not mitigate field-scale N2O emissions in a Northern California

vineyard: an assessment across two years. Agric. Ecosyst. Environ. 191, 27–38.

Vistoso, E., Alfaro, M., Saggar, S., Salazar, F., 2012. Effect of nitrogen inhibitors on nitrous oxide emissions

and pasture growth after an autumn application in volcanic soil. Chil. J. Agric. Res. 72, 133–139.

Vitale, L., Ottaiano, L., Polimeno, F., Maglione, G., Amato, U., Arena, C., Di Tommasi, P., Mori, M., Magliulo,

V., 2013. Effects of 3,4-dimethylphyrazole phosphate-added nitrogen fertilizers on crop growth and N2O

emissions in Southern Italy. Plant Soil Environ. 59, 517–523.

Zhu-Barker, X., Horwath, W.R., Burger, M., 2015. Knife-injected anhydrous ammonia increases yield-scaled

N2O emissions compared to broadcast or band-applied ammonium sulfate in wheat. Agr. Ecosyst. Environ.

212, 148–157.